Detecting whitefish divergence
using remains of Cladocerans in
lake sediment
Tracking shifts in the predation regime on Bosmina by
measuring defense structures
Anna Swärd
Student
Degree Thesis in Biology 15 ECTS Bachelor’s Level
Abstract
Predation by northern pike is believed to have initiated a divergence in whitefish into several different morphs, differing in size, habitat use and growth rate. The development of a small pelagic zooplankton feeding morph is expected to have large impacts on the zooplankton community. In this study the effect of a changing predation regime on Bosmina, before and after introduction of pike in Valsjön, was investigated. By looking at the change in carapace length (and indication of the level of predation pressure from fish) and mucro index (an indication of the level of invertebrate predation) of Bosmina remains in lake sediment the changing predation pressure from invertebrates and fish could be investigated. These features proved to be good proxys for the level of defense against fish and invertebrate predation. However, other species than whitefish, and unknown interactions seems to have affected the zooplankton community. This makes it hard to tell which effect is due to
diversification in whitefish and which is not. Also it is not clear that it is pike that has induced the divergence in the whitefish population. Other species like brown trout might also have been involved.
Key Words: Bosmina, Leptodora, Bythotrephes, pike, whitefish, predation, resource
Table of contents
1 Introduction
... 1
1.1 Background ... 1
1.2 Purpose ... 3
1.3 Study site: lakeValsjön ... 3
2. Materials and methods
... 5
2.1 Sediment sampling and dating ... 5
2.2 Cladocera preparations, counting and measurement ... 5
1. Introduction
1.1 Background
European whitefish, Coregonus lavaretus (L.) is a common freshwater species in Europe. In many lakes several different monophyletic sub-species or morphs are found (Svärdson 1953, 1979), which often differ in habitat use, food selection and growth rate (Bergstrand 1982, Amundsen 1988). This sympatric ecological speciation is believed to be initiated by predation (Öhlund 2012); the presence of northern pike (Esox Lucius) seems to induce divergence from one littoral generalist whitefish species into different ecotypes. The ecotypes are often consisting of one large bodied, littoral benthivore morph with few, sparse gill rakers and a small bodied pelagic planktivore morph with many, dense gill rakers (Kahilainen et al. 2003, 2005, Jensen et al. 2008, Öhlund et al. unpublished). Even though pike is only one of several potential predators of whitefish, it stands out as being primarily littoral and having a gap size large enough to catch relatively large prey (Vøllestad et al. 1986, Mittelbach 1998). The emergence of different whitefish ecotypes can be relatively quick after introduction of northern pike, with the probability to detect diverging reaching 50% after only 72 years, representing approximately 18 generations, and the ecotypes continue to diverge genetically over time (Öhlund 2012). In many cases, reproductive isolation is indicated by the fact that small and large ecotypes segregate in time or space during spawning (Svärdson 1979). Body size and size at maturation are plastic traits which often diverge rapidly, whereas gill raker number is genetically determined (Rogers and Bernatches 2007) and diverge much slower. According to Öhlund (2012) pike might induce a life history trade-off. Either whitefish are forced to 1) stay safely in the pelagic with low scope for growth, due to a diet solely consisting of zooplankton, and thus mature early at a small size, or 2) to move to the littoral habitat, with higher predation risk, but with high scope for growth due to more large bodied benthic prey, and thus mature later at a larger size. The reduced feeding efficiency of large individuals of whitefish, due to problems with handling small food items, may cause a shift from feeding on zooplankton to feeding on large benthic invertebrates. Only then can they be able to sustain positive growth when they get bigger (Kahilainen 2003). This niche shift can be beneficial for large whitefish because they can grow out of the predation window if the presence of predators in the littoral zone reduces densities of smaller competitors (Persson et al. 1996).
There seems to be a clear correlation between gill raker traits, feeding behavior and food preferences. Sparsely raked forms are in general benthivores, whereas the densely raked whitefish forms are planktivores (Svärdson 1979, Bergstrand 1982, Amundsen 1988, Amundsen et al. 2004 b).
Zooplankton are considered excellent indicators of aquatic food web structure, due to their role as grazers on primary producers and their sensitivity to predation both by fish and invertebrates. Several key zooplankton taxa also leave identifiable remains preserved in lake sediments, providing an opportunity to track changes in predation pressure over time (Korosi et al. 2013). Bosmina remains are often highly abundant in lake sediment and because these species often undergo cyclomorphosis in response to predation by fish and invertebrates, measurements of sub fossil Bosmina features can indicate predation regime shifts (Korosi et al. 2013).
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because their invertebrate predators are highly preyed upon and less abundant (Post et al. 1995).
The presence of a small bodied whitefish morph in a polymorph whitefish lake affect small zooplankton, like Bosmina, both directly and indirectly (Bartels et al. unpublished). In monom0rphic lakes, the competition for zooplankton resources in the pelagic habitat is weak and zooplankton are large-bodied, abundant and diverse (Kahilainen et al. 2011). Individual growth rate in monomorph whitefish is high for immature and low for mature fish (Pruuki 1982, Skurdal et al. 1985, Olajos 2013). This makes it reasonable to assume that whitefish is reproduction limited (Persson et al. 2013). Strong competition for benthos then leads to reduced reproduction in adults, which leads to less competition in juveniles and makes them grow fast and reach a size where they do not affect the zooplankton resource any more. When a proportion of the fish community is adapting to a zooplankton resource, this leads to increased competition for, and thus increased predation pressure on zooplankton, which is indicated by reduced body size and density of zooplankton (Amundsen et al. 2004 a, Kahilainen et al. 2007). This provides a feedback loop that further strengthens the selection pressure on fish towards smaller body size and higher foraging efficiency on small prey items (Kahilainen et al. 2011).
Pelagic invertebrate predators are highly preferred prey for planktivorus fish including coregonids (Langeland 1978, Fitzmaurice 1979, Mookerji et al. 1998, Palmer et al. 2001), but different invertebrate species experience differential predation pressure by fish. Body size divergence in whitefish has been suggested to induce a change in the dominance pattern of predatory invertebrates (Bartels et al. unpublished). This can have substantial impacts on herbivorous zooplankton because predatory invertebrates are able to remove large portions of zooplankton production (Lunte and Luecke 1990, Herzig 1995). A study by Bartels et al. (unpublished) found that body size divergence in whitefish determined the dominance of two important invertebrate predators and that the changes in predatory invertebrate composition mediated by fish further influenced small zooplankton communities (figure 1). In the study it was found that lakes without pike and with monomorphic whitefish were dominated by
Bythotrephes, whereas lakes with pike were dominated by Leptodora. In pike-less lakes,
predation on pelagic predatory invertebrates is expected to be weak due to the preferential consumption of macroinvertebrates by large whitefish (Bartels et al. unpublished).
Bythotrephes is the better competitor of the two and can sometimes even prey on Leptodora
(Branstrator 1995, 2005), resulting in the dominance of the former when predation is weak (Bartels et al. unpublished). In pike lakes, small whitefish exert strong predation on invertebrate predators. However, they preferably consume Bythotrephes over Leptodora, which is less susceptible to fish predation due to its high body transparency (Palmer et al. 2001). Leptodora is a highly efficient invertebrate predator of small-bodied, filter-feeding cladocerans like Daphnia and Bosmina (Browman et al. 1989 Lunte and Luecke 1990, Branstrator and Lehman 1991). The size range of prey that can be consumed by Leptodora is limited by the size of the feeding basket (formed by the thoracic limbs) in which prey is captured. Morphologic characters that increase the overall size of their prey, such as large carapace and long appendages, are expected to be favored under high predation by
Leptodora (Korosi et al. 2013). Bythotrephes on the other hand prefers small to medium
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Figure 1. Conceptual figure describing effects on the zooplankton community caused by large-bodied monomorphic whitefish and small-bodied whitefish found in lakes with polymorphic whitefish. Dashed lines mean weak interactions, solid thin lines mean medium strong interactions and solid thick lines means strong interactions (Bartels 2014).
1.2 Purpose
The purpose of this study is to examine if Bosmina remains in lake sediments can be used as a proxy for the historical presence of northern pike in Valsjön in north western Jämtland. Based on the studies cited above and historical records presented below, I hypothesized that the introduction of pike in lake Valsjön induced divergence in body size of whitefish into two different morphs, one large, littoral benthivore and one small pelagic planktivore. In this way the introduction of pike and the ensuing diversification of whitefish is expected to affect zooplankton community and size structure directly through predation and indirect by removal of invertebrate predators (Bartels et al. unpublished), leading to a shift from mainly large, undefended zooplankton, to small and more defended ones. Information about historic change in the level of defense in zooplankton, against both invertebrate and fish predators, can hopefully be used in future studies to detect the time of pike introduction or whitefish divergence in lakes where the timing of these events is unknown.
1.3 Study site: lake Valsjön
The location of this study is lake Valsjön in north western Jämtland in Sweden (lat 64,02˚N, long 14,21˚E). The lake has an area of 919 ha. Mean depth is 20,7 m and maximum depth is 72 m (SMHI 2014).
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vendance (Coregonus albula) in Valsjön (PIKE 2014). This is however highly unlikely given the high altitude and the fact that vendance is not found in any of the nearby lakes (Svärdson 1998). More likely is that there were already two different whitefish morphs in the lake at this time. In 1905 the species composition in Valsjön was almost the same as in 1896, but there was also alpine bullhead (Cottus poecilopus) and European perch (Perca fluviatilis), but no Eurasian ruffe (PIKE 2014). Today the lake harbors two different whitefish morphs (figure 2) along with, pike, perch, brown trout, burbot, grayling and European minnow (Öhlund 2014 pers.com.). Mean fork length of the small whitefish morph is 151,3 mm (SE ±2,3) and the mean fork length of the large morph is 302 mm (SE ±2,4). Mean gill raker number of the small morph is 41,3 (SE ±0,2) and mean gill raker number of the large morph is 41,7 (SE ±0,2).
The zooplankton taxa present today in Valsjön and their biomasses are given in table 1.
Figure 2. Fork length and number of gill rakers for whitefish sampled from Valsjön in 2013.
Table 1. Abundance and biomass of different zooplankton taxa in Valsjön from August 2013.
Taxa Abundance (ind/1000L) Biomass (mg/1000L)
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2. Materials and methods
2.1 Sediment sampling and dating
A sediment core, 40 cm long and 6 cm in diameter, was taken in Valsjön on the 9th of April 2013 using an UWITEC core sampler. The core was taken near the deepest point of the lake, at 68,5 meters. The sediment was sliced in smaller sections immediately after collection. The first 20 cm of the sample was sliced into 0,5 cm sections starting at the surface and the deeper sections were sliced in 1 cm sections. The sediment sections were collected in plastic boxes and stored in a cold room (8˚C) until analysis in April 2014. The chronology of the sediments was obtained by applying 210Pb dating. The half-life of the natural radionuclide 210Pb is (T1/2 =22.3 years) and its chemical properties make it suitable for establishing the chronology of archives accumulated over approximately the past 150 years. 210Pb activities were determined by alpha-spectrometry measuring the activities of 210Po, assumed in secular equilibrium (Sánchez-Cabeza et al. 1998). The mean sedimentation rate was obtained by applying the CF:CS model (constant flux: constant sedimentation), which assumes constant sediment accumulation rates (Krishnaswami 1971, Appleby 2001). This value was used to estimate the ages of each layer of the sediment record. Through extrapolation also the ages of deeper (older than 150 years) layers could be estimated.
2.2 Cladocera preparations, counting and measurement
Approximately 0.2 g of freeze-dried sediment from every forth section between section 1 and section 40, and every second section between section 42 and 50 was measured with an analytical scale. Each sediment sample was mixed with 100 ml of 10% potassium hydroxide (KOH) and transferred to a hot plate at 100°C until boiling. Samples were kept at approximately 85°C for another 30 minutes. Subsequently, samples were removed from the hot plate and mixed with tap water for cooling. Treating the sediment with KOH degrades organic material, resulting in a “clean” sample that is dominated by cladoceran remains. When cooled down, samples were first sieved through a 35µm sieve and rinsed with tap water. The samples was further sieved through a 100µm sieve and transferred to a 15 ml falcon tube. The residuum was transferred to a 50 ml falcon tube. Two to three drops of the biological stain safranin-glycerol was added to all falcon tubes. In this study, only the 100µm samples were further processed. A known volume (between 3 and 4 ml, depending on the amount of cladoceran remains) from each 15 ml falcon tube was transferred to a 10 ml sediment chamber. Using an OLYMPUS microscopes equipped with a digital camera, pictures of cladoceran were taken. Although the pictures contained remains of other cladoceran genera, most remains belonged to the genus Bosmina, which is the main focus of this study. Bosmina body and mucro length were measured (Figure 3) and the number of heads and bodies were counted using the image analysis software Guppy 1.0.
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3. Results
Bosmina carapace length (figure 4) increased in the older sediment sections until around 170
years ago suggesting a decreased predation level. From then, and up to around 100 years ago there is a decrease, suggesting increased predation level. After that there is little change until about 40 years ago, when carapace length starts decreasing again indicating a higher level of fish predation.
Figure 4. Mean carapace length of Bosmina with standard error. Horizontal bars indicate 95% confidence interval for estimates of year.
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Figure 5. Mean mucro index of Bosmina with standard error. The estimation of years are displayed with 95% confidence interval.
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Figure 6. Abundance of Bosmina in each core section, estimated as the number of heads /0.2 g dried sediment.
The estimation of years are displayed with 95% confidence interval.
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4. Discussion
4.1 Whitefish divergence
Whitefish has been present in Valsjön at least since 1794 (Burman 1794). The first records of pike being present in Valsjön is from 1896 (Lundberg 1899) and the first indication of polymorphism in whitefish is from 1905 (PIKE 2014). According to Ericsson (1932) pike was however not common in Valsjön until after the construction of the log driving channel between Sausjön and Valsjön, most likely sometime around 1920. Today there is both pike and two whitefish morphs in Valsjön. Based on this information it can be assumed that the whitefish in Valsjön evolved two morphs sometime between 1794 and 1905. The results from measurments of Bosmina carapace length show a clear decreasing trend for most of this time. The mucro index however is more variable, and shows a decreasing trend from the 1870s to around 1900. From the beginning of the last century both carapace length and mucro index is almost unchanged for more than 50 years. However after 1974 both mucro index and carapace length follows a pattern expected in a polymorphic whitefish lake, with increased mucro length and decreasing body size indicating increased predation pressure both from fish and predatory invertebrates.
Even if the data on changing Bosmina morphology shows some trends, one can only speculate about when the two morphs in Valsjön has emerged and what could have caused the divergence. Sympatric speciation in whitefish seems to, in many cases, have been initiated by the introduction of Northern pike (Öhlund et al. unpublished). However, also in lakes without pike there can be polymorphic whitefish populations, even if this is rare (Öhlund et al. unpublished). Another, very recently developed hypothesis, which has not yet been tested, suggests that the presence of large brown trout might have the same ability to induce whitefish divergence as pike (Öhlund 2014 pers.com.). Brown trout is a common top-predator in many north European lakes, particularly in systems dominated by coregonid fish, and may reach a large body size through piscivory (Næsje et al. 1998, Vehanen et al. 1998). A study by Jensen et al. (2008) stated that large trout (>20 cm), may feed almost exclusively on coregonid fish. Even if they usually prefer small prey, large individuals of brown trout are able to catch even fairly large whitefish prey (Jensen et al. 2008). Valsjön is known for harboring a stock of large brown trout (Fellsman 2008, Fiskeinfo 2014). The large river Hårkan, which runs through Valsjön, provides suitable spawning areas for large adult trout. There is also the possibility that the divergence of whitefish occurred without the influence of predation by pike or brown trout. A widespread view is that divergence in northern lakes occurred after the last ice age in response to intense intraspecific competition and abundant ecological opportunities (Skulason and Smith 1995, Bolnick 2004, Siwertsson et al. 2010, Kahilainen et al. 2011).
4.2 Bosmina defense
The emergence of two different whitefish morphs is expected to have strong effects on the zooplankton community because the small-bodied morph is an efficient planktivore (Amundsen et al. 2004 a, Bartels et al. unpublished, Kahilainen et al. 2007). Small cladocerans like Bosmina, can be affected both directly and indirectly (Bartels et al. unpublished). The Bosmina population is expected to experience a decrease in body size due to direct predation from the small whitefish (Bartels et al. unpublished) and the indirect effect is expected to be caused by the increased predation pressure from the small whitefish on invertebrate predators which according to Bartels et al. (unpublished) will lead to a shift in the dominance pattern from Bythotrephes to Leptodora. According to Branstrator and Lehman (1991), Leptodora seem to be a more effective predator on Bosmina than
Bythotrephes, which will reduce the density of Bosmina (Browman et al. 1989, Lunte and
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In figure 4, the decreasing carapace length from around 1840 could be interpreted as an indication of increasing predation pressure from fish. This increased predation pressure could be a result of the development of two different whitefish morphs, with the emergence of a small pelagic zooplankton specialist. If this is true one can speculate that pike was present in Valsjön earlier than 1896 and that the emergence of two morphs actually happened much earlier than 1905, when it was first noted. It is also possible that the divergence in whitefish was not caused by pike, but by brown trout. Especially considering that pike does not seem to have been common in Valsjön until after the construction of the log driving channel (Ericsson 1932). However, the relatively strong decreasing trend stops and levels out around 1920. After mid 1970s the trend is again decreasing until present. This pattern is a bit difficult to explain with the hypothesis that there has been a constant predation pressure from the small whitefish morph at this time.
The decreasing mucro index from the 1870s to the beginning of the 1900s (figure 5) is indicating that the predation pressure from invertebrate predators (i.e. Leptodora) was decreasing at this time. This could be due to a dominance of Bythotrephes among invertebrate zooplankton, which is the opposite of what would be expected with a small whitefish morph present in the lake at this time.
A possible explanation to the trends in Bosmina defense levels before the 1920s involves the Arctic char. An introduction of whitefish, around the end of the 18th century could have led to strong competition for zooplankton with sympatric Arctic char. Whitefish is responsible for partially or completely displacing many native Arctic char populations, evidently because its better ability to utilize pelagic food resources (Nilsson and Pejler 1973, Svärdson 1976). Whitefish are able to feed on smaller zooplankton than Arctic char, and can selectively graze zooplankton populations down to levels where Arctic char can no longer feed efficiently (Johnston 2002). This increased predation pressure on zooplankton could explain the decreased carapace length observed in Bosmina from the 1840s to around 1920. The Arctic char disappears from Valsjön, sometime after the introduction of pike. It was present in the lake in 1905 (PIKE 2014), but is gone today (Öhlund 2014 pers.com.). Arctic char rarely coexist with pike, which act as both a predator and competitor (Byström et al. 2007, Spens and Ball 2008). Whitefish is expected to experience competitive release with the Arctic char gone. This could explain why the predation pressure from fish seems to level out from around 1920 (or maybe earlier) to the mid-1970s (figure 5), and the decreasing predation pressure from invertebrate predators seems to level out from approximately the same time to sometime after the end of the 1950s. When the Arctic char is gone, an increase in the predation pressure from pike on whitefish might have been initiated, resulting in the divergence towards two different morphs.
With the two morphs present in the lake the small morph starts to exert a stronger predation pressure on the zooplankton community affecting Bosmina both directly through increased predation, and indirectly through an increased predation pressure on invertebrate predators. This is consistent with the trends in figure 4 and 5 which indicate smaller carapace length and an increased mucro index in Bosmina. From the data one can see a decrease in body size of Bosmina, indicating stronger predation pressure by fish, and a higher mucro index, indicating stronger predation pressure from invertebrate predators, around the mid-seventies.
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4.3 Bosmina density
A common finding is that a high density of specialized planktivorous fish cause a decrease in zooplankton body size and density (Nilsson and Pejler 1973, Post et al. 2008). Kahilainen et al. (2011) found that zooplankton body size and density decreased with increasing coregonid diversity. These findings are also supported by Bartels et al (unpublished), who studied several lakes in northern Sweden, including Valsjön. They found in two out of three lake pairs, that that total biomass of small zooplankton was lower in lakes with pike and polymorphic whitefish than in lakes with monomorphic whitefish and no pike. But pike-less lakes was dominated by Daphnia, whereas pike lakes were dominated by Bosmina.
The number of Bosmina heads in sediment from Valsjön show strong fluctuations and there is no clear correlation with the decreasing carapace length of Bosmina (figure 7), suggesting no direct impact on fish predation on Bosmina demography. The density of Bosmina can however go through large natural fluctuations over time (Briones et al. 2012). These large natural fluctuations might exceed and disguise changes caused by shifting predation regimes in longer time series.
4.4 Conclusions
The purpose of this study was to use Bosmina remains in lake sediment as a proxy for the historical presence of northern pike in Valsjön in north western Jämtland. This has proven to be a bit difficult. Also other species and unknown interactions seem to have affected the zooplankton community. This makes it hard to tell which effect is due diversification in whitefish and which is not. Also it is not clear that it is pike that has induced the divergence in the whitefish population. Other species like brown trout might have been involved. To be able to evaluate the influence of pike in shaping the zooplankton community indirectly through causing a divergence in the whitefish stock, a comparison with the upstream lake Gunnarvattnet will probably give more answers. Gunnarvattnet has no pike because of migration barriers. It would also be interesting to examine remains of Daphnia and compare these with data on Bosmina. In pike less lakes Daphnia is expected to dominate over
Bosmina, but in pike lakes it is expected to be the other way around (Bartels et al.
unpublished). Today Bosmina is the dominating species (table 1.), but it would be interesting to compare the abundance of the two species to see if there has been a shift, and in that case when it happened. If it is possible to find remains of Bytotrepehes and Leptodora, it would be very interesting to study changes in the dominance pattern of these species.
Bosmina remains seems to be a very useful tool for detecting historical changes in predation
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5. Acknowledgements
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Dept. of Ecology and Environmental Science (EMG) S-901 87 Umeå, Sweden
